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Ranaviruses Evolutionary Intermediate Within Common The Genome Sequence of the Emerging Common Midwife Toad Virus Identifies an Evolutionary Intermediate within Ranaviruses Carla Mavian, Alberto López-Bueno, Ana Balseiro, Rosa Casais, Antonio Alcamí and Alí Alejo J. Virol. 2012, 86(7):3617. DOI: 10.1128/JVI.07108-11. Published Ahead of Print 1 February 2012. Downloaded from Updated information and services can be found at: http://jvi.asm.org/content/86/7/3617 These include: http://jvi.asm.org/ REFERENCES This article cites 41 articles, 6 of which can be accessed free at: http://jvi.asm.org/content/86/7/3617#ref-list-1 CONTENT ALERTS Receive: RSS Feeds, eTOCs, free email alerts (when new articles cite this article), more» on April 5, 2012 by UNIV OF MAINE Information about commercial reprint orders: http://jvi.asm.org/site/misc/reprints.xhtml To subscribe to to another ASM Journal go to: http://journals.asm.org/site/subscriptions/ The Genome Sequence of the Emerging Common Midwife Toad Virus Identifies an Evolutionary Intermediate within Ranaviruses Carla Mavian,a Alberto López-Bueno,a Ana Balseiro,b Rosa Casais,b Antonio Alcamí,a and Alí Alejoc* Centro de Biología Molecular Severo Ochoa (CSIC-UAM), Universidad Autónoma de Madrid, Madrid, Spaina; Centro de Biotecnología Animal, Servicio Regional de Investigación y Desarrollo Agroalimentario, Gijón, Spainb; and Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Valdeolmos, Spainc Worldwide amphibian population declines have been ascribed to global warming, increasing pollution levels, and other factors directly related to human activities. These factors may additionally be favoring the emergence of novel pathogens. In this report, we have determined the complete genome sequence of the emerging common midwife toad ranavirus (CMTV), which has caused fatal disease in several amphibian species across Europe. Phylogenetic and gene content analyses of the first complete genomic Downloaded from sequence from a ranavirus isolated in Europe show that CMTV is an amphibian-like ranavirus (ALRV). However, the CMTV genome structure is novel and represents an intermediate evolutionary stage between the two previously described ALRV groups. We find that CMTV clusters with several other ranaviruses isolated from different hosts and locations which might also be included in this novel ranavirus group. This work sheds light on the phylogenetic relationships within this complex group of emerging, disease-causing viruses. http://jvi.asm.org/ lobal population declines and extinction of multiple amphib- been published only for Asian, American, and Australian isolates Gian species have been reported over the last 20 years (11). As (18, 21, 24, 28, 35, 37, 41). Recently, it has been proposed that estimated by the International Union for Conservation of Nature, ranaviruses can be subdivided into two distinct groups based on the Amphibia class includes the highest number of critically en- phylogenetic analyses and genome colinearity, grouper iridovirus dangered species among the animal classes examined, with an es- (GIV)-like ranaviruses and amphibian-like ranaviruses (ALRV) timated 41% of its species under threat (23). Therefore, this class (24). The first group includes GIV and Singapore grouper irido- seems to be a particularly sensitive indicator of the current biodi- virus (SGIV), which were isolated in Asia from fish (35, 41). The versity losses associated with the global warming process and ALRVs include frog virus 3 (FV3) and Ambystoma tigrinum virus on April 5, 2012 by UNIV OF MAINE other human-related environmental factors. It has been shown (ATV), which were isolated from frogs and salamanders, respec- that habitat loss, increased human population density, and in- tively, in North America, the tiger frog virus (TFV), isolated in creased climatic variability are important factors that compromise China, the epizootic hematopoietic necrosis virus (EHNV), iso- the survival of amphibian species (34) and that multiple drivers of lated from fish in Australia, and the soft-shelled turtle iridovirus extinction are likely to coordinately accelerate amphibian declines (STIV), isolated in China (21). Within the ALRVs, the degree of in the near future (20). genome sequence colinearity is high, although two different The role of emerging infectious diseases in the rapid decline of groups of viruses can be distinguished: the EHNV/ATV group, amphibian populations is being increasingly studied. The recent which may be closer to a putative most recent common ancestor of spread of the lethal fungal pathogen Batrachochytrium dendroba- the whole group (24), and the FV3/TFV/STIV group, which shows tidis is well documented and has been associated with long-term two discrete acquired genomic inversions when compared to the amphibian population declines in several locations (6). A second genomes of the former group. widespread pathogen of amphibians that is now recognized as an Ranavirus emergence as a pathogen of amphibians and other emerging infectious disease and therefore likewise included in the ectothermic vertebrates is probably linked to their host range plas- list of notifiable diseases by the World Organization for Animal ticity as well as to environmental and ecological factors (17). The Health is ranaviruses. Although their association with population first clear evidence that viral infection can be the cause of localized declines has to be studied further (14), ranavirus infections have amphibian population declines was reported in Europe, where been clearly associated with mass mortalities of several amphibian ranaviruses have caused large-scale mortalities of the common as well as reptile and fish species worldwide (3, 36, 40). frog Rana temporaria in the United Kingdom since 1985 (40). The Ranavirus is a genus within the Iridoviridae family which in- causative agent is thought to be a variant of FV3, which may have cludes large, icosahedral viruses containing circular, double- stranded DNA genomes with sizes ranging from 105 kbp to 140 kbp and a coding potential of approximately 100 open reading Received 14 December 2011 Accepted 18 January 2012 frames (ORFs) (10). The family includes five different genera, two Published ahead of print 1 February 2012 of which infect insects while the others infect cold-blooded verte- Address correspondence to Alí Alejo, [email protected]. brates. Species from the genera Megalocytivirus and Lymphocysti- * Present address: Centro de Investigación en Sanidad Animal (INIA), Ctra. de virus have been found to infect only teleost fish, while ranaviruses Algete a El Casar, Valdeolmos, Spain. are known to infect reptiles, amphibians, and fish, and the reasons C. Mavian and A. López-Bueno contributed equally to this article. for this broad host specificity are yet unknown. Copyright © 2012, American Society for Microbiology. All Rights Reserved. Ranavirus outbreaks have been described from different loca- doi:10.1128/JVI.07108-11 tions worldwide. However, full-length genome sequences have 0022-538X/12/$12.00 Journal of Virology p. 3617–3625 jvi.asm.org 3617 Mavian et al. been introduced through the movement of infected animals from previously annotated in other ranaviral genomes, preserving the same North America (22). number for both R and L orientations (CMTV ORFs 35 and 54). The common midwife toad virus (CMTV) was first isolated on Nucleotide-to-nucleotide comparisons between the CMTV genome and the European continental mainland in 2007 from diseased tad- other iridoviral genomes as well as among different ranaviruses were cal- poles of the common midwife toad (Alytes obstetricans) in a high- culated using the JDotter (Java Dot Plot Alignments) software with the altitude permanent water trough in the Picos de Europa National default settings. The algorithm employed by this software is described in detail in reference 9. In the dot plots generated, a straight line represents a Park in Spain (4). The virus, causing a high mortality rate in this stretch of similarity between the two sequences compared on the x and y species as well as in juvenile alpine newts in the 2008 outbreak axes. The full-length genome sequences (accession numbers) used in (Mesotriton alpestris cyreni) (5), was shown to be responsible for a the dot plot analyses were FV3 (AY548484), TFV (AF389451), ATV systemic hemorrhagic disease. Common histological findings (AY150217), EHNV (FJ433873), GIV (AY666015), SGIV (AY521625), were the presence of intracytoplasmic inclusion bodies and the and STIV (NC012637). Phylogenetic trees were constructed using necrosis of endothelial cells, the latter of which results in destruc- MEGA5 software. For the phylogenetic analysis of ranavirus MCPs, the tion of several organs, including skin, liver, and kidney. Sequence following sequences were used: ranavirus KRV-1 (KRV-1; accession no. analyses of DNA fragments belonging to the major capsid protein ADO14139), Rana catesbeiana virus-JP (RCV-JP; no. BAH80413), soft- Downloaded from (MCP) and DNA polymerase genes showed that CMTV clustered shelled turtle iridovirus (STIV; no. ABC59813), frog virus 3 (FV3; no. more closely with the ALRVs than with the GIV-like ranaviruses ACP19256), tiger frog virus (TFV; no. AAK55105), Bohle iridovirus (BIV; no. ACO90022), pike-perch iridovirus (PPIV; no. ACO90019), Rana within the Ranavirus genus. In 2010, a CMTV outbreak in a pond esculenta virus (REV; no. ACO90020), Chinese giant salamander virus in the Netherlands was described as the cause of a mass mortality (CGSV; no. ADZ47908), Ambystoma tigrinum virus (ATV; no. event affecting
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